Christine Ferrier-Pagès

Heterotrophy in Tropical Scleractinian Corals

The dual character of corals, that they are both auto‐ and heterotrophs, was recognized early in the twentieth Century. It is generally accepted that the symbiotic association between corals and their endosymbiotic algae (called zooxanthellae) is fundamental to the development of coral reefs in oligotrophic tropical oceans because zooxanthellae transfer the major part of their photosynthates to the coral host (autotrophic nutrition). However, numerous studies have confirmed that many species of corals are also active heterotrophs, ingesting organisms ranging from bacteria to mesozooplankton. Heterotrophy accounts for between 0 and 66% of the fixed carbon incorporated into coral skeletons and can meet from 15 to 35% of daily metabolic requirements in healthy corals and up to 100% in bleached corals. Apart from this carbon input, feeding is likely to be important to most scleractinian corals, since nitrogen, phosphorus, and other nutrients that cannot be supplied from photosynthesis by the coral’s symbiotic algae must come from zooplankton capture, particulate matter or dissolved compounds. A recent study showed that during bleaching events some coral species, by increasing their feeding rates, are able to maintain and restore energy reserves.

Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata

Abstract The effect of prolonged (9 week) nutrient enrichment on the growth and photosynthetic rates of the zooxanthellate coral Stylophora pistillata was investigated. The main questions were: (1) what is the exposure time needed to induce measurable change in growth rate? (2) which are the concentrations of nitrogen and phosphorus required to cause changes in these rates? (3) what is the recovery potential of the corals after the nutrient stress? For this purpose, three tanks (N, P, NP) were enriched with ammonium (N), phosphorus (P) or both nutrients (NP), respectively. A fourth tank (C) served as a control. The growth of 40 nubbins (10 in each tank) was monitored during four periods: period 1 (nutrient-poor conditions), period 2 (10 μm NH4 and/or 2 μm PO4 enrichment), period 3 (20 μm NH4 and/or 2 μm PO4) and period 4 (nutrient-poor conditions). Period 4 was performed to study the recovery potential of corals after a nutrient stress. During period 1, growth rates remained constant in all tanks. In the P tank, growth rates declined during the two enrichment periods, with a total decrease of 60% by the end of period 3. In the N tank, growth rates remained nearly constant during period 2 but decreased in period 3 (60% decrease). In the NP tank, 50% and 25% decreases were observed during periods 2 and 3. At the end of the recovery period, a regain in growth rate was observed in the N and NP tanks (35 and 30% increase, respectively, compared with the rates measured at the end of period 3) and growth rates returned to 60% of the initial rates. By contrast, in the P tank, there was no regain in growth and a further decrease of 5% was observed. Rates of photosynthesis were often higher during the enriched than the nutrient-poor period (up to 150% increase). Corals with the highest percent increases in maximal gross photosynthetic rate (Pgmax) had the smallest decreases in growth rate due to nutrient enrichment. In conclusion, high ammonium (20 μm) and relatively low phosphorus concentrations (2 μm) are required to induce a significant decrease in coral growth rate. The largest reduction was observed with both ammonium and phosphorus enrichment. The decrease in growth rate was rapid following nutrient enrichment, since a 10% decrease or more could be observed after the first week of treatment.

Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison.

Biogenic calcification is influenced by the concentration of available carbonate ions. The recent confirmation of this for hermatypic corals has raised concern over the future of coral reefs because [CO32−] is a decreasing function of increasing pCO2 in the atmosphere. As one of the overriding features of coral reefs is their diversity, understanding the degree of variability between species in their ability to cope with a change in [CO32−] is a priority. We cultured four phylogenetically and physiologically different species of hermatypic coral (Acropora verweyi, Galaxea fascicularis, Pavona cactus and Turbinaria reniformis) under ‘normal’ (280 mu;mol kg−1) and ‘low’ (140 μmol kg−1) carbonate–ion concentrations. The effect on skeletogenesis was investigated quantitatively (by calcification rate) and qualitatively (by microstructural appearance of growing crystalline fibres using scanning electron microscopy (SEM)). The ‘low carbonate’ treatment resulted in a significant suppression of calcification rate and a tendency for weaker crystallization at the distal tips of fibres. However, while the calcification rate was affected uniformly across species (13–18%reduction), the magnitude of the microstructural response was highly species specific: crystallization was most markedly affected in A. verweyi and least in T. reniformis. These results are discussed in relation to past records and future predictions of carbonate variability in the oceans.

Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata

This work investigated the effect of light and feeding on tissue composition as well as on rates of photosynthesis and calcification in the zooxanthellae (zoox) scleractinian coral, Stylophora pistillata. Microcolonies were maintained at three different light levels (80, 200, 300 μmol m−2 s−1) and subjected to two feeding regimes (starved and fed) over 9 weeks. Corals were fed both natural plankton and Artemia salina nauplii four times a weeks and samplings were made after 2, 5, and 9 weeks. Results confirmed that feeding enhances coral growth rate and increases both the dark and light calcification rates. These rates were 50–75% higher in fed corals (FC; 60±20 and 200±40 nmol Ca2+ cm−2 h−1 for dark and light calcification, respectively) compared to control corals (CC; 30±9 and 124±23 nmol Ca2+ cm−2 h−1). The dark calcification rates, however, were four times lower than the rates of light calcification (independent of trophic status). After 5 weeks, chlorophyll a (chl-a) concentrations were four to seven times higher in fed corals (7–21 μg cm−2) than in control corals (2–5 μg cm−2). The amount of protein was also significantly higher in fed corals (2.11–2.50 mg cm−2) than in control corals (1.08–1.52 mg cm−2). Rates of photosynthesis in fed corals were 2–10 times higher (1.24±0.75 μmol O2 h−1 cm−2) than those measured in control corals (0.20±0.08 μmol O2 h−1 cm−2).

Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata

SUMMARY We investigated the effect of zooplankton feeding on tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Microcolonies were divided into two groups: starved corals (SC), which were not fed during the experiment, and fed corals (FC), which were abundantly fed with Artemia salina nauplii and freshly collected zooplankton. Changes in tissue growth, photosynthesis and calcification rates were measured after 3 and 8 weeks of incubation. Calcification is the deposition of both an organic matrix and a calcium carbonate layer, so we measured the effect of feeding on both these parameters, using incorporation of 14C-aspartic acid and 45Ca, respectively. Aspartic acid is one of the major components of the organic matrix in scleractinian corals. For both sampling times, protein concentrations were twice as high in FC than in SC (0.73 vs 0.42 mg P–1 cm–2 skeleton) and chlorophyll c2 concentrations were 3–4 times higher in fed corals (2.1±0.3 μg cm–2). Cell specific density (CSD), which corresponds to the number of algal cells inside a host cell, was also significantly higher in FC (1.416±0.028) than in SC (1.316±0.015). Fed corals therefore displayed a higher rate of photosynthesis per unit area (Pgmax= 570±60 nmol O2 cm–2 h–1 and Ik=403±27 μmol photons m–2 s–1). After 8 weeks, both light and dark calcification rates were twofold greater in FC (3323±508 and 416±58 nmol Ca2+ 2 h–1 g–1 dry skeletal mass) compared to SC (1560±217 and 225±35 nmol Ca2+ 2 h–1 g–1 dry skeletal mass, respectively, under light and dark conditions). Aspartic acid incorporation rates were also significantly higher in FC (10.44±0.69 and 1.36± 0.26%RAV 2 h–1 g–1 dry skeletal mass, where RAV is total radioactivity initially present in the external medium) than in SC (6.51±0.45 and 0.44±0.02%RAV 2 h–1 g–1 dry skeletal mass under dark and light conditions, respectively). Rates of dark aspartic acid incorporation were lower than the rates measured in the light. Our results suggest that the increase in the rates of calcification in fed corals might be induced by a feeding-stimulation of organic matrix synthesis.

The Symbiotic Anthozoan: A Physiological Chimera between Alga and Animal.

Abstract The symbiotic life style involves mutual ecological, physiological, structural, and molecular adaptations between the partners. In the symbiotic association between anthozoans and photosynthetic dinoflagellates (Symbiodinium spp., also called zooxanthellae), the presence of the endosymbiont in the animal cells has constrained the host in several ways. It adopts behaviors that optimize photosynthesis of the zooxanthellae. The animal partner has had to evolve the ability to absorb and concentrate dissolved inorganic carbon from seawater in order to supply the symbionts photosynthesis. Exposing itself to sunlight to illuminate its symbionts sufficiently also subjects the host to damaging solar ultraviolet radiation. Protection against this is provided by biochemical sunscreens, including mycosporine-like amino acids, themselves produced by the symbiont and translocated to the host. Moreover, to protect itself against oxygen produced during algal photosynthesis, the cnidarian host has developed certain antioxidant defenses that are unique among animals. Finally, living in nutrient-poor waters, the animal partner has developed several mechanisms for nitrogen assimilation and conservation such as the ability to absorb inorganic nitrogen, highly unusual for a metazoan. These facts suggest a parallel evolution of symbiotic cnidarians and plants, in which the animal host has adopted characteristics usually associated with phototrophic organisms.

Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms

BackgroundCoral bleaching can be defined as the loss of symbiotic zooxanthellae and/or their photosynthetic pigments from their cnidarian host. This major disturbance of reef ecosystems is principally induced by increases in water temperature. Since the beginning of the 1980s and the onset of global climate change, this phenomenon has been occurring at increasing rates and scales, and with increasing severity. Several studies have been undertaken in the last few years to better understand the cellular and molecular mechanisms of coral bleaching but the jigsaw puzzle is far from being complete, especially concerning the early events leading to symbiosis breakdown. The aim of the present study was to find molecular actors involved early in the mechanism leading to symbiosis collapse.ResultsIn our experimental procedure, one set of Pocillopora damicornis nubbins was subjected to a gradual increase of water temperature from 28°C to 32°C over 15 days. A second control set kept at constant temperature (28°C). The differentially expressed mRNA between the stressed states (sampled just before the onset of bleaching) and the non stressed states (control) were isolated by Suppression Subtractive Hybridization. Transcription rates of the most interesting genes (considering their putative function) were quantified by Q-RT-PCR, which revealed a significant decrease in transcription of two candidates six days before bleaching. RACE-PCR experiments showed that one of them (PdC-Lectin) contained a C-Type-Lectin domain specific for mannose. Immunolocalisation demonstrated that this host gene mediates molecular interactions between the host and the symbionts suggesting a putative role in zooxanthellae acquisition and/or sequestration. The second gene corresponds to a gene putatively involved in calcification processes (Pdcyst-rich). Its down-regulation could reflect a trade-off mechanism leading to the arrest of the mineralization process under stress.ConclusionUnder thermal stress zooxanthellae photosynthesis leads to intense oxidative stress in the two partners. This endogenous stress can lead to the perception of the symbiont as a toxic partner for the host. Consequently, we propose that the bleaching process is due in part to a decrease in zooxanthellae acquisition and/or sequestration. In addition to a new hypothesis in coral bleaching mechanisms, this study provides promising biomarkers for monitoring coral health.

Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata.

SUMMARY This study was designed to assess the importance of dissolved free amino acids (DFAA) as a nitrogen source for the scleractinian coral Stylophora pistillata. For this purpose, experiments were performed using 15N-enriched DFAAs, and %15N enrichment was measured both in animal tissue and zooxanthellae at different DFAA concentrations, incubation time and light levels. As previously observed for urea, which is another source of organic nitrogen, DFAA uptake exhibited a biphasic mode consisting of an active carrier-mediated transport for concentrations below 3μ mol l–1 and a linear uptake for higher concentrations. The value of the carrier affinity (Km=1.23 μmol l–1 DFAA) indicated good adaptation of the corals to the low levels of DFAA concentrations measured in most oligotrophic waters. DFAA uptake was also correlated with light. The DFAA contribution to the nitrogen requirements for tissue growth was compared to the contribution of ammonia, nitrate and urea, for which uptake was also measured in S. pistillata. Inorganic sources (NH4+ and NO3–) contributed 75% of the daily nitrogen needs against 24% for organic sources. Taken altogether, dissolved organic and inorganic nitrogen can supply almost 100% of the nitrogen needs for tissue growth.

Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation

SUMMARY Corals live in symbiosis with dinoflagellates of the genus Symbiodinum. These dinoflagellates translocate a large part of the photosynthetically fixed carbon to the host, which in turn uses it for its own needs. Assessing the carbon budget in coral tissue is a central question in reef studies that still vexes ecophysiologists. The amount of carbon fixed by the symbiotic association can be determined by measuring the rate of photosynthesis, but the amount of carbon translocated by the symbionts to the host and the fate of this carbon are more difficult to assess. In the present study, we propose a novel approach to calculate the budget of autotrophic carbon in the tissue of scleractinian corals, based on a new model and measurements made with the stable isotope 13C. Colonies of the scleractinian coral Stylophora pistillata were incubated in H13CO –3-enriched seawater, after which the fate of 13C was followed in the symbionts, the coral tissue and the released particulate organic carbon (i.e. mucus). Results obtained showed that after 15 min, ca. 60% of the carbon fixed was already translocated to the host, and after 48 h, this value reached 78%. However, ca. 48% of the photosynthetically fixed carbon was respired by the symbiotic association, and 28% was released as dissolved organic carbon. This is different from other coral species, where <1% of the total organic carbon released is from newly fixed carbon. Only 23% of the initially fixed carbon was retained in the symbionts and coral tissue after 48 h. Results show that our 13C-based model could successfully trace the carbon flow from the symbionts to the host, and the photosynthetically acquired carbon lost from the symbiotic association.

Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures.

SUMMARY The Ligurian Sea (NW Mediterranean) experienced warm summers in 1998, 1999 and from 2003 to 2005. The temperature was 1-3°C higher than the mean summer value (24°C) and remained high over a long period. During these summers, mass-mortality events, affecting several sessile benthic species, were reported. In the present study, we tested the long-term (3-7 weeks) effect of different temperatures (20°C measured in spring and autumn, 24°C observed in summer, and 26°C and 28°C abnormal summer values) on two Mediterranean corals, Cladocora caespitosa and Oculina patagonica. Growth rate, photosynthetic efficiency (Fv/Fm), relative electron transport rate (ETR), zooxanthellae and chlorophyll (chl) contents were measured during 48 days incubation. At 20°C, all parameters remained constant during the whole experiment for both species. At higher temperatures, most physiological parameters were affected by only 2-5 weeks at 24°C, and were severely depressed at higher temperatures. Small replicate samples (nubbins) of O. patagonica significantly decreased their zooxanthellae and chl concentrations at all temperatures, after 2 weeks of incubation. Their Fv/Fm values, as well as their growth rates, were also gradually reduced during the incubation at all temperatures. However, only a few nubbins maintained at 28°C showed signs of tissue necrosis after 34 days, and these gradually recovered tissue when temperature was returned to normal. In nubbins of C. caespitosa, chl and zooxanthellae concentrations decreased only after 34 days of incubation at 26°C and 28°C. At the same time, tissue necrosis was observed, explaining the loss of the symbionts. Fv/Fm was reduced only after 34 days of incubation at the different temperatures, and growth rate was first enhanced, before collapsing by 30% at 24°C and by 90-100% at 26°C and 28°C. All samples maintained at 26°C and 28°C had died, due to tissue necrosis, by the end of the experiment. Results obtained suggest that O. patagonica is more able than C. caespitosa to resist high temperature conditions because of its rapid bleaching capacity. In contrast, it seems that C. caespitosa is living close to its thermal limit during the summer period; therefore, a long-term increase at 24°C or above could be lethal for this coral, just as was observed in situ during the recent warm summers.